Qi-Cai Chen

Preceding weak noise sharpens the frequency tuning and elevates the response threshold of the mouse inferior collicular neurons through GABAergic inhibition.

In acoustic communication, animals must extract biologically relevant signals that are embedded in noisy environment. The present study examines how weak noise may affect the auditory sensitivity of neurons in the central nucleus of the mouse inferior colliculus (IC) which receives convergent excitatory and inhibitory inputs from both lower and higher auditory centers. Specifically, we studied the frequency sensitivity and minimum threshold of IC neurons using a pure tone probe and a weak white noise masker under forward masking paradigm. For most IC neurons, probe-elicited response was decreased by a weak white noise that was presented at a specific gap (i.e. time window). When presented within this time window, weak noise masking sharpened the frequency tuning curve and increased the minimum threshold of IC neurons. The degree of weak noise masking of these two measurements increased with noise duration. Sharpening of the frequency tuning curve and increasing of the minimum threshold of IC neurons during weak noise masking were mostly mediated through GABAergic inhibition. In addition, sharpening of frequency tuning curve by the weak noise masker was more effective at the high than at low frequency limb. These data indicate that in the real world the ambient noise may improve frequency sensitivity of IC neurons through GABAergic inhibition while inevitably decrease the frequency response range and sensitivity of IC neurons.

The auditory response properties of single-on and double-on responders in the inferior colliculus of the leaf-nosed bat, Hipposideros armiger.

The present study examines the response properties of neurons in the central nucleus of the inferior colliculus (IC) of the CF-FM (constant frequency-frequency-modulated) bat, Hipposideros armiger using CF, FM and CF-FM sounds as stimuli. All 169 IC neurons recorded are tonotopically organized along the dorsoventral axis of the IC. Collicular neurons have V-shaped or upper-threshold frequency tuning curves. Those neurons tuned at the predominant second harmonic have extremely sharp frequency tuning curves and low minimum thresholds. Collicular neurons typically discharge impulses to both CF and FM sounds. However, when stimulated with CF-FM sounds, most (76%) neurons only discharge impulses to the onset of CF-FM sounds (single-on responders). The remaining neurons (24%) discharge impulses to both CF and FM components (double-on responders) of CF-FM sounds. The double-on responders have higher minimum threshold and longer latency to the FM component than to the CF component of CF-FM sounds. Our data show that the FM component of the CF-FM sounds contributes significantly in shaping the discharge pattern, latency and number of impulses of IC neurons. The present study suggests that using CF-FM sounds to study auditory response properties of the CF-FM bat may be essential for a better understanding of echo analysis by the CF-FM in the real world. Because the double-on responders have shorter response latency than single-on responders, we speculate that these two types of responders may be best suited for echo analysis during different phases of hunting.

The recovery cycle of bat duration-selective collicular neurons varies with hunting phase.

During hunting, duration selectivity and recovery cycle underlie a bats ability to determine echo duration and target distance (echo ranging). This study shows that the recovery cycle of most duration-selective neurons in the bat central nucleus of the inferior colliculus neurons varies with biologically relevant pulse–echo (P–E) duration and amplitude. As such, neurons with short best duration recover rapidly when stimulated with P–E pairs with short duration and small P–E amplitude difference, whereas neurons with long best duration recover rapidly when stimulated with P–E pairs with long duration and large P–E amplitude difference. These data indicate that different groups of duration-selective neurons underlie the bats ability to effectively perform echo recognition and ranging during different phases of hunting.

THE EFFECT OF PULSE REPETITION RATE, PULSE INTENSITY, AND BICUCULLINE ON THE MINIMUM THRESHOLD AND LATENCY OF BAT INFERIOR COLLICULAR NEURONS

This study examines the effect of pulse repetition rate (PRR), pulse intensity, and bicuculline on the minimum threshold (MT) and latency of inferior collicular neurons of the big brown bat, Eptesicusfuscus, under free-field stimulation conditions. It tests the hypothesis that changes in MT and latency of collicular neurons are co-dependent on PRR. The number of impulses in inferior collicular neurons (n = 245) increased either monotonically (25%) or non-monotonically (75%) with pulse intensity. Latencies either decreased to a plateau (72%), fluctuated unpredictably within 3 ms (21%) or changed very little (7%) with increasing pulse intensity. Latencies and MTs of most collicular neurons increased by 1.5–24 ms (mean ± SD = 4.8 ± 3.3 ms) and 4–75 dB (mean ± SD = 22.1 ± 16.2 dB) with increasing PRR. In most neurons (94%), the latency increase was completely (42%) or partially (52%) eliminated when pulse intensity was compensated for the MT increase with PRR. Complete elimination of latency was achieved by bicuculline application. In a few neurons (6%), the latency increase with PRR was not affected by compensated pulse intensity or bicuculline application.

Bilateral Collicular Interaction: Modulation of Auditory Signal Processing in Amplitude Domain

In the ascending auditory pathway, the inferior colliculus (IC) receives and integrates excitatory and inhibitory inputs from many lower auditory nuclei, intrinsic projections within the IC, contralateral IC through the commissure of the IC and from the auditory cortex. All these connections make the IC a major center for subcortical temporal and spectral integration of auditory information. In this study, we examine bilateral collicular interaction in modulating amplitude-domain signal processing using electrophysiological recording, acoustic and focal electrical stimulation. Focal electrical stimulation of one (ipsilateral) IC produces widespread inhibition (61.6%) and focused facilitation (9.1%) of responses of neurons in the other (contralateral) IC, while 29.3% of the neurons were not affected. Bilateral collicular interaction produces a decrease in the response magnitude and an increase in the response latency of inhibited IC neurons but produces opposite effects on the response of facilitated IC neurons. These two groups of neurons are not separately located and are tonotopically organized within the IC. The modulation effect is most effective at low sound level and is dependent upon the interval between the acoustic and electric stimuli. The focal electrical stimulation of the ipsilateral IC compresses or expands the rate-level functions of contralateral IC neurons. The focal electrical stimulation also produces a shift in the minimum threshold and dynamic range of contralateral IC neurons for as long as 150 minutes. The degree of bilateral collicular interaction is dependent upon the difference in the best frequency between the electrically stimulated IC neurons and modulated IC neurons. These data suggest that bilateral collicular interaction mainly changes the ratio between excitation and inhibition during signal processing so as to sharpen the amplitude sensitivity of IC neurons. Bilateral interaction may be also involved in acoustic-experience-dependent plasticity in the IC. Three possible neural pathways underlying the bilateral collicular interaction are discussed.

Recovery Cycle of Neurons in the Inferior Colliculus of the FM Bat Determined with Varied Pulse-Echo Duration and Amplitude

The recovery cycle of auditory neurons is an important neuronal property which underlies a bats ability in analyzing returning echoes and to determine target distance (i.e., echo ranging). In the same token, duration selectivity of auditory neurons plays an important role in pulse recognition in bat echolocation. Because insectivorous bats progressively vary the pulse parameters (repetition rate, duration, and amplitude) during hunting, the recovery cycle of auditory neurons is inevitably affected by their selectivity to other co-varying echo parameters. This study examines the effect of pulse duration and amplitude on recovery cycle of neurons in the central nucleus of the inferior colliculus (IC) of the FM bat, Pipistrellus abramus, using biologically relevant pulse-echo (P-E) pairs with varied duration and amplitude difference. We specifically examine how duration selectivity may affect a neurons recovery cycle. IC neurons have wide range of recovery cycle and best duration (BD) covering P-E intervals and duration occurring different phases of hunting. The recovery cycle of most IC neurons increases with P-E duration and amplitude difference. Most duration-selective IC neurons recover rapidly when stimulated with biologically relevant P-E pairs. As such, neurons with short BD recover rapidly when stimulated with P-E pairs of short duration and small P-E amplitude difference. Conversely, neurons with long BD recover rapidly when stimulated with P-E pairs of long duration and large P-E amplitude difference. These data suggest that bats may potentially utilize the response of IC neurons with different BD and recovery cycle to effectively perform echo detection, recognition of echo duration and echo ranging throughout a target approaching sequence.

Bilateral collicular interaction: Modulation of auditory signal processing in frequency domain

In the ascending auditory pathway, the inferior colliculus (IC) receives and integrates excitatory and inhibitory inputs from a variety of lower auditory nuclei, intrinsic projections within the IC, contralateral IC through the commissure of the IC and the auditory cortex. All these connections make the IC a major center for subcortical temporal and spectral integration of auditory information. In this study, we examine bilateral collicular interaction in the modulation of frequency-domain signal processing of mice using electrophysiological recording and focal electrical stimulation. Focal electrical stimulation of neurons in one IC produces widespread inhibition and focused facilitation of responses of neurons in the other IC. This bilateral collicular interaction decreases the response magnitude and lengthens the response latency of inhibited IC neurons but produces an opposite effect on the response of facilitated IC neurons. In the frequency domain, the focal electrical stimulation of one IC sharpens or expands the frequency tuning curves (FTCs) of neurons in the other IC to improve frequency sensitivity and the frequency response range. The focal electrical stimulation also produces a shift in the best frequency (BF) of modulated IC (ICMdu) neurons toward that of electrically stimulated IC (ICES) neurons. The degree of bilateral collicular interaction is dependent upon the difference in the BF between the ICES neurons and ICMdu neurons. These data suggest that bilateral collicular interaction is a part of dynamic acoustic signal processing that adjusts and improves signal processing as well as reorganizes collicular representation of signal parameters according to the acoustic experience.

Local neuronal circuits that may shape the discharge patterns of inferior collicular neurons

The discharge patterns of neurons in auditory centers encode information about sounds. However, few studies have focused on the synaptic mechanisms underlying the shaping of discharge patterns using intracellular recording techniques. Here, we investigated the discharge patterns of inferior collicular (IC) neurons using intracellular recordings to further elucidate the mechanisms underlying the shaping of discharge patterns. Under in vivo intracellular recording conditions, recordings were obtained from 66 IC neurons in 18 healthy adult mice (Mus musculus, Km) under free fi eld-stimulation. Fiftyeight of these neurons fi red bursts of action potentials (APs) to auditory stimuli and the remaining eight just generated local responses such as excitatory (n = 4) or inhibitory (n = 4) postsynaptic potentials. Based on the APs and subthreshold responses, the discharge patterns were classifi ed into seven types: phasic (24/58, 41.4%), phasic burst (8/58,13.8%), pauser (4/58, 6.9%), phasic-pauser (1/58, 1.7%), chopper (2/58, 3.4%), primary-like tonic (14/58, 24.1%) and sound-induced inhibitory (5/58,8.6%). We concluded that (1) IC neurons exhibit at least seven distinct discharge patterns; (2) inhibition participates in shaping the discharge pattern of most IC neurons and plays a role in sculpting the pattern, except for the primary-like tonic pattern which was not shaped by inhibition; and (3) local neural circuits are the likely structural basis that shapes the discharge patterns of IC neurons and can be formed either in the IC or in lower-level auditory structures.

Modulation of amplitude sensitivity by bilateral collicular interaction among different frequency laminae.

In the ascending auditory pathway, the commissure of the inferior colliculus (IC) interconnects the two ICs and may therefore mediate bilateral collicular interaction during sound processing. In this study, we show that electrically stimulates one IC produces facilitation or suppression of acoustically evoked response of neurons in the other IC. The facilitated IC neurons (14%) are located in bilateral corresponding frequency laminae while the suppressed IC neurons (86%) are widespreadly located in bilateral different frequency laminae. Whereas induced facilitation increases the dynamic range but decreases the slope of the rate-amplitude function of modulated IC neurons, induced suppression produces the opposite effect. As a result, bilateral collicular facilitation increases the sensitivity of modulated IC neurons to a wider range of sound amplitude while bilateral collicular suppression improves the sensitivity of modulated IC neurons to minor change in sound amplitude over a narrower range of sound amplitude. The degree of suppression is significantly greater for suppressed IC neurons located in bilateral corresponding frequency laminae than in non-corresponding frequency laminae. We suggest that bilateral collicular interaction through the commissure of the IC may play a role in modulation of amplitude sensitivity and in shaping the binaural property of IC neurons.

Role of frequency band integration in sharpening frequency tunings of the inferior colliculus neurons in the big brown bat,Eptesicus fuscus

By means of a particular two-tone stimulation paradigm in combination of using a pair of electrodes for simultaneously recording from two inferior colliculus (IC) neurons, the currentin vivo study is undertaken to explore the role of frequency band integration (FBI) in sharpening of frequency tuning in the big brown bat,Eptesicus fuscus. Three major results are found: (1) The paired neurons correlated to FBI are located not only within the same frequency filter bandwidth (FFB), but also across different FFBs. The relations of their frequency tuning curves (FTCs) are mainly of two types: the flank-overlapped and overlaid patterns. (2) Although the sharpness of FTCs between paired neurons is mutual, the sharpening efficiency of neurons located within the same FFB is higher than that of neurons across FFBs, and the FTCs of neurons with the best frequencies (BF) of 20 –30 kHz are most strongly sharpened. (3) The strength of FBI is weak near the BF but gradually increased with frequencies away from the BF of sound stimuli. This suggests that the dynamical FBI of the IC neurons located within and across the FFBs might be involved in the formation of functional FFB structures.